Bradleya 24/2006 39

Summary: The genus Micranthocereus includes

nine endemic Brazilian species distributed in the

states of Bahia, Minas Gerais, Goiás and

Tocantins. In the present study the floral biology

of M. flaviflorus, M. steckeri and M. purpureus

from “campo rupestre” vegetation of the Chapada

Diamantina, Bahia, was investigated. Data on

floral morphology and nectar production (concen-

tration and volume) were collected throughout

anthesis. Flowers of all species are tubular and

present coloured perianth-segments. Nectar is

accumulated within a nectar-chamber, located

inside the floral tube. Flowers of M. flaviflorus

and M. streckeri are predominantly nocturnal,

opening in the night (at about 7 p.m.). Each

flower lasts c.36 hours, with a concentration of

sugar in the nectar between approximately

18–24%. Both species present floral features typ-

ical for ornithophily, and were pollinated by the

hummingbird Clorostilbon aureoventris, whose

visits occurred in regular intervals and were

characterized by territorialist behaviour. Species

of bees and butterflies were also observed visiting

flowers of M. flaviflorus and M. streckeri. M.

streckeri was additionally visited by the hum-

mingbird Phaethornis squalidus, mainly in the

afternoon. Flowers of M. purpureus are noctur-

nal, and each flower lasts c.17 hours and present

longer corollas with wider diameter than those of

the other two species studied; sugar concentra-

tion in the nectar was about 21–22%. Three

sphingid and one bat species were observed visit-

ing flowers of M. purpureus, with a greater fre-

quency of visits of the sphingids. Pollen viability

was high (80–90%) and similar between the three

species of Micranthocereus studied.

Zusammenfassung: Die Gattung Micran-

thocereus umfasst neun in Brasilien endemische

Arten, und ist in den Bundesstaaten Bahia,

Minas Gerais, Goiás und Tocantins verbreitet. In

der vorliegenden Arbeit wurde die Blütenbiologie

der Arten M. flaviflorus, M. purpureus und

M. streckeri aus den “campos rupestres”

(Felssavannen) der Chapada Diamantina (Bahia)

untersucht. Während der gesamten Blühphase

wurden Daten über Blütenmorphologie und

Nektarproduktion (Konzentration und Volumen)

gesammelt. Die Blüten aller Arten sind

röhrenförmig and haben ein farbiges Perianth.

Der Nektar sammelt sich in der Nektarkammer,

die sich im Inneren der Blütenröhre befindet. Die

Blüten von M. flaviflorus and M. streckeri sind

hauptsächlich nachts geöffnet. Die Anthese

beginnt abends gegen ungefähr 19.00. Eine Blüte

dauert etwa 36 Stunden und hat eine

Zuckerkonzentration im Nektar zwischen

18–24%. Beide Arten weisen Blütenmerkmale

auf, die typisch für Vogelblumen sind. Sie

wurden von der Kolibriart Clorostilbon

aureoventris bestäubt, dessen Besuche in

regelmässigen Intervallen erfolgten und durch

BBrraaddlleeyyaa 2244//22000066pages 39 – 52

PPoolllliinnaattiioonn bbiioollooggyy ooff tthhrreeee BBrraazziilliiaann ssppeecciieess ooff MMiiccrraanntthhoocceerreeuussBBaacckkeebb.. ((CCeerreeeeaaee,, CCaaccttooiiddeeaaee)) eennddeemmiicc ttoo tthhee ““ccaammppoossrruuppeessttrreess””

Lidyanne Yuriko Saleme Aona1, Marlon Machado2, Emerson Ricardo Pansarin1,Cibele Cardoso de Castro3, Daniela Zappi4 and Maria do Carmo E. do Amaral11Dept. de Botânica, IB, Universidade Estadual de Campinas, Caixa Postal 6109, Cidade Universitária s.n.,13084-970, Campinas-SP, Brazil (email: lidyanne.aona@gmail.com).2University of Zurich, Institute for Systematic Botany, Zollikerstrasse 107, CH-8008, Zurich, Switzerland.3Departamento de Biologia, Universidade Federal Rural de Pernambuco R. Dom Manoel de Medeiros, s/n- Dois Irmãos, 52171-900, Recife-Pernambuco, Brazil. 4Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, UK.

Bradleya 24/200640

territoriales Verhalten gekennzeichnet waren.

Ausserdem wurden verschiedene Arten von

Bienen und Schmetterlingen bei Blütenbesuchen

von M. flaviflorus und M. streckeri beobachtet.

Besonders am Nachmittag wurde M. streckeri

zusätzlich von der Kolibriart Phaethornis

squalidus besucht. M. purpureus ist

nachtblühend, und jede Blüte bleibt etwa 17

Stunden geöffnet. Ihre Blütenröhren sind länger

und weisen auch einen grösseren Durchmesser

auf als diejenigen der beiden anderen Arten. Die

Zuckerkonzentration des Nektars betrug

21–22%. Drei Arten von Schwärmern und eine

Fledermausart wurden bei Blütenbesuchen

beobachtet, wobei die Schwärmer häufigere

Besuche zeigten als die Fledermäuse. Die

Lebensfähigkeit des Pollens aller drei

untersuchten Arten war hoch und betrug ca.

80–90%.

Resumo: O gênero Micranthocereus inclui nove

espécies endêmicas do Brasil e restritas aos

Estados da Bahia, Minas Gerais, Goiás e

Tocantins. Foi estudada a biologia floral de

M. flaviflorus, M. steckeri e M. purpureus em

campos rupestres na Chapada Diamantina, BA.

Análises da morfologia floral e medições do

volume e concentração do néctar desde a antese

até o pré-fenescimento das flores foram

realizadas. As flores das três espécies estudadas

são tubulares, apresentando segmentos do

perianto diversamente coloridos. O néctar é

armazenado na câmara nectarífera, localizada no

interior do tubo floral. As flores de M. flaviflorus

e M. streckeri apresentam antese noturna,

abrindo no início da noite (aproximadamente 7

horas da noite). Cada flor dura cerca de 36 horas

e apresenta concentração de açúcares entre 18 e

24%. Ambas as espécies apresentam

características típicas de flores polinizadas por

aves e são visitadas e polinizadas pela mesma

espécie de beija-flor, Clorostilbon aureoventris. As

visitas ocorreram em intervalos regulares e o

beija-flor apresentou comportamento

territorialista, quando dois indivíduos visitavam

simultaneamente as flores. Visitas de abelhas e

borboletas também foram observadas nestas

espécies. M. streckeri também foi visitado por

outro beija-flor, Phaethornis squalidus, que

efetuou um maior número de visitas no período

vespertino. As flores de M. purpureus

apresentam antese noturna, e cada flor dura

aproximadamente 17 horas. O comprimento e

diâmetro floral são superiores aos das espécies

diurnas e a concentração de açúcares varia entre

21 e 22%. Foram observadas visitas de três

espécies de esfingídeos e de uma espécie de

morcego. Foi observada uma maior freqüência de

visitas dos esfingídeos em relação ao morcego. O

teste de viabilidade polínica foi semelhante entre

as espécies estudadas (80–90%).

IInnttrroodduuccttiioonn

The family Cactaceae forms a monophyletic

group (Wallace & Cota, 1996) with approximate-

ly 100 genera and 1300 species distributed near-

ly exclusively in the New World (Barthlott &

Hunt, 1993). Eastern Brazil presents the third

main geographical centre of diversity of the fam-

ily (Zappi, 1994; Taylor & Zappi, 2004). The core

geographical area defined within Eastern Brazil

has been recognized primarily for its remarkable

endemism of Cactaceae genera and species, espe-

cially those of the “caatingas” of the North-east-

ern states and associated highland known as

“campos rupestres” (Taylor & Zappi, 2004).

Cactaceae present a wide range of floral fea-

tures regarding shape, colour, size, odour, time of

anthesis and position of the reproductive parts,

which indicate pollination by several groups of

biotic agents (Porsch, 1939; Hunt & Taylor, 1990;

Vogel, 1990), like medium-sized (McFarland et

al., 1989) and large bees (Viana et al., 2001),

sphingids and other moths (Suzan et al., 1994;

Holland & Fleming, 1999), hummingbirds

(Scobell & Scott, 2002), bats (Ruiz et al., 1997;

Tschapka et al., 1999), or even nocturnal and

diurnal vectors in the same species, such as by

hummingbirds and bats (Fleming et al., 1996;

Sahley, 2001). According to Vogel (1990), around

9% of the species of Cactaceae are pollinated by

hummingbirds. Other studies on Cactaceae also

reported several reproductive strategies like self-

compatibility (Bianchi et al., 2000) and self-

incompatibility (Boyle, 1996; Metz et al., 2000),

as well as the presence of sexual and asexual

reproduction in the same species (Mandujano et

al., 1998; Negron-Ortiz, 1998).

The Brazilian genus Micranthocereus Backeb.

(Cactoideae, Cereeae) includes nine species dis-

tributed in the states of Minas Gerais, Bahia,

Goiás and Tocantins (Taylor & Zappi, 2004).

Studies concerning the reproductive biology of

Brazilian Cactaceae recorded melitophily in

Opuntia Mill. (Schlindwein & Wittmann, 1995,

1997), sphingophily in Cereus Mill. (Silva &

Sazima, 1995; Locatelli & Machado, 1999a) and

Selenicereus (Berg.) Britton & Rose (Barthlott et

Bradleya 24/2006 41

al., 1997), ornithophily in Melocactus Link &

Otto and Opuntia (Locatelli & Machado, 1999b;

Raw, 1996), and chiropterophily in Pilosocereus

Byles & Rowley (Locatelli et al., 1997). The repro-

ductive biology of Micranthocereus species is

unknown, but the genus presents great diversity

in flower morphology.

The main goal of this study was to investigate

and compare the pollination biology of three

Brazilian Micranthocereus species: M. flaviflorus

Buining & Brederoo, M. streckeri van Heek & van

Criekinge and M. purpureus (Gürke) Ritter

endemic to northeast Brazil.

MMaatteerriiaall aanndd MMeetthhooddss

The floral biology of the species studied was

investigated in the Chapada Diamantina (Bahia

State), a mountain complex that presents a large

diversity of Cactaceae species (Machado, 1999;

Taylor & Zappi, 2004) and which is located in the

Cadeia do Espinhaço, a mountain range which

extends over c.1000 km from NE to SE Brazil.

The study was conducted in August 2001 for M.

flaviflorus and M. streckeri and in October 2003

for M. purpureus.

The studied population of M. flaviflorus con-

sisted of c. 20 individuals located in the munici-

pal district of Morro do Chapéu (10°50’S–12°00’S

and 40°40’W–41°30’W)1

. The plants grow in

quartzitic sand in an area occupied by transition-

al vegetation including ‘cerrado’ (savanna),

‘campo rupestre’ (upland or highland savanna)

and ‘caatinga’ (deciduous low thorn forest). The

population of M. streckeri consisted of 40 individ-

uals and was located upon rocks in an area of

‘campo rupestre’ vegetation surrounded by forest

areas, being endemic to the study area, in the

Municipality of Seabra (12º25’52S and

41º59’36W). M. purpureus presents a much larg-

er distribution range, occurring from Rio de

Contas to Jacobina (Aona, 2003). The population

studied consisted of 40 individuals and is located

in the Municipality of Morro do Chapéu

(11º36’03S and 41º09’52W), occurring in an area

of ‘campo rupestre’ vegetation.

The growth habit, phenology and floral fea-

tures, such as morphology, colour and scent, were

recorded through field observation. Floral lifes-

pan and anthesis events were recorded for a pop-

ulation of each species through the observation of

tagged flowers from pre-anthesis until flower

senescence. Fresh flowers of each species were

randomly collected in a minimum of 15–30 indi-

viduals/species, fixed in FAA 50, stored in alcohol

70% and used for illustrations and for floral mea-

surements (flower-tube length and diameter,

17–32 flowers/species). Floral measurements

were obtained with a digital calliper (error 0.01

mm) and compared between species with an

ANOVA analysis coupled with a t-Test LSD

(Sokal & Rohlf, 1969).

Nectar concentration and volume were esti-

mated in flowers bagged from the pre-anthesis

stage, using a pocket refractometer and micro-

liter syringes, respectively. Data were collected c.

24 hours after the beginning of the anthesis for

M. flaviflorus (n=12 flowers) and M. streckeri

(n=10 flowers, five individuals for both), and 3

hours (n=10, eight individuals) and 9 hours (n=8,

six individuals) after anthesis for M. purpureus.

Pollen viability was estimated using the acetate-

carmine technique (Radford et al., 1974, 5-7 flow-

ers/species, 200 pollen grains/flower).

Floral visitors were recorded through direct

observations in the field, in a total of 10h for

M. flaviflorus, 40h for M. streckeri and 40h for

M. purpureus. Time and duration of visiting

bouts were recorded, as well as the visitor’s

behaviour on the flowers, such as contact with

the anthers and the stigma, type of floral

resource collected and interactions with other

visitors. Buds/mature flowers were tagged in the

afternoon and examined early in the morning for

detecting possible nocturnal pollination in

M. flaviflorus and M. streckeri. The humming-

birds were identified in the field and using pho-

tographs taken during their visits, then com-

pared with ilustrations in Ruschi (1986) and

Grantsau (1989).

Others floral visitors of M. purpureus were

identified using photos taken during their visits

to the flowers; these photos were also used to

check the sites of pollen deposition on their bod-

ies. Insect visitors of all species were collected

and identified as far as possible through compar-

ison with specimens deposited in the Museum of

the Universidade Estadual of Campinas (ZUEC).

Pollinators were characterized based on their fre-

quency of visits and visiting behaviour.

Frequency of visits of the main floral visitors of

1

This population belongs to the taxon recently recognized as M. polyanthus (Werderm.) Backeb. subsp. alvinii M. Machado &

Hofacker. These plants are to some degree intermediate between M. flaviflorus and M. polyanthus (Werderm.) Backeb. which are

similar species (Taylor & Zappi, 2004: 355).

Bradleya 24/200642

each species was compared using a Student’s t

test (Sokal & Rohlf, 1969).

Voucher specimens were deposited in the

Herbarium of the Universidade Estadual de

Campinas (M. flaviflorus: UEC 120736,

M. streckeri: UEC 139459 and M. purpureus UEC

132282).

RReessuullttss

MMoorrpphhoollooggyy aanndd fflloorraall bbiioollooggyy

The plants of all studied species are columnar,

branching at the base, with decumbent or erect

stems and covered with flexible, golden to pale

golden spines. Flowers are born in a specialized

fertile zone (cephalium), more or less perpendicu-

lar and lateral to the stem axis. The flowers pre-

sent a nectariferous chamber with a nectary

inside the base of the flower-tube, where the nec-

tar is produced and accumulated (Figures 1–3).

All the species presented high pollen viability

(77–90%) which is similar between species

(F=3.35, P=0.06).

In M. flaviflorus and M. streckeri the fertile

zone consists of a lateral, superficial to sunken

cephalium with flower-bearing areoles, which

have white to yellowish hairs with long, pale to

brownish golden bristles in M. flaviflorus, and

compact, white to brownish hairs and long, pale

golden to reddish brown bristles in M. streckeri.

In M. purpureus, the fertile portion of the stem is

a lateral cephalium sunken into the stem and

composed of congested flower-bearing areoles

which bear pale brown, pinkish or grey, abun-

dant, loose or compact hair and few long golden

or brownish bristles.

M. flaviflorus flowered from May to

September and produced fruits from July to

November, whereas M. streckeri produced flowers

from May to September and fruits from August to

December. Both species present an annual

3mm

3mm

FFiigguurree 11. Longitudinal section of flower of M. flavi-florus. Note the nectar chamber (arrow). Illustrationby R. Lupo.

FFiigguurree 22. Longitudinal section of flower of M. streck-eri. Note the nectar chamber (arrow). Illustration byR. Lupo.

Bradleya 24/2006 43

flowering pattern (sensu Newstron et al., 1994).

Flowers of M. flaviflorus have outer perianth-

segments spreading to erect, reddish pink; the

inner perianth-segments opened very slightly

and are yellow to pale cream (Figures 4 & 5);

those of M. streckeri have outer perianth-seg-

ments spreading and deep pink, the inner peri-

anth-segments are erect and purplish pink

(Figures 6–9). The flowers of both species are

tubular, the stamens are positioned inside the

floral tube; the stigma is 4- to 6-lobed, and the

stigma-lobes are also inserted (Figures 1–3).

Flower length of M. flaviflorus (12.3 ± 0.1mm,

mean ± SE) was smaller than that of M. streckeri

(13.1 ± 1.2mm, mean ± SE, t=-2.618, P=0.01,

n=32 for both), whereas the diameter was similar

(1.8 ± 0.2mm for M. flaviflorus, 1.8 ± 0.9mm for

M. streckeri, mean ± SE, t=-1.593, P>0.01, n=32

for both, 1).

Flowers of M. flaviflorus and M. streckeri

started to open at about 7 p.m. (5–10 flowers each

individual daily), and lasted c.36 hours, wilting

in the morning of the third day. In recently

opened flowers the stigma-lobes were closed and

the pollen was released; between the end of the

first day and the beginning of the second day of

the anthesis, the stigma-lobes opened and

became perceptibly moist. The flowers of both

species were scentless and produced similar nec-

tar volumes, whereas the concentration of sugar

was higher in M. flaviflorus (Table 1).

The flowering period of M. purpureus

occurred from May to November, and the plants

developed fruits between July and December,

indicating an annual flowering pattern (sensu

Newstron et al., 1994). The floral tube of M. pur-

pureus is deep pink-magenta, the outer perianth-

segments are recurved and deep pink to reddish;

the inner perianth-segments are spreading or

recurved, white. The stamens are numerous

(c.400), being disposed as a dense ring inside the

tube. The style is long, tube-like and exceeds the

anthers by about 10mm; the exerted stigma is 10-

lobed. Flowers are larger than those of the other

two species (F=793.64 for corolla length and

F=239.81 for corolla diameter, P=0 for both,

Table 1).

Individuals of Micranthocereus purpureus

opened 2-3 flowers each in the afternoon (5 p.m.),

which reached full anthesis 2 hour later,

remained open during the night, and were com-

pletely closed by 10–11 a.m. the next morning.

When the flower was completely open, the stig-

mas were moist (indicating receptivity), laterally

or adaxially displaced; after c. 2 hours it began to

move slowly towards the center of the flower,

where it remained until the end of anthesis.

The flowers of M. purpureus presented a

slightly sweet and sour scent. Sugar concentra-

tion in the nectar decreased during the period

between 8 p.m. and 2 a.m. Nectar volume was

higher in M. purpureus than in the other two

species (F=142.16, P=0), which presented similar

volume values (P=0.21); on the other hand, the

highest nectar concentration was observed in M.

flaviflorus, being followed by M. purpureus and

M. streckeri (F=18.29, P<0.05 for all comparisons,

Table 1).

PPoolllliinnaattiioonn pprroocceessss

The main floral visitors of Micranthocereus flavi-

florus were males of the hummingbird

Chlorostilbon aureoventris Boucier & Mulsant

(Figure 4), which were observed from early morn-

ing until 2 p.m. This hummingbird visited the

flowers at regular intervals of approximately

10–30 minutes. The females visited the flowers

only sporadically, being frequently chased away

by the males during the visits. Chlorostilbon

aureoventris has a straight bill (19.09 ± 2.1mm

length, mean ± SE, n = 5), that contacted the

5mm

FFiigguurree 33. Longitudinal section of flower of M. pur-pureus. Note the nectar chamber (arrow). Illustrationby R. Lupo.

Bradleya 24/200644

FFiigguurree 44. Female of Chlorostilbon aureoventris visiting flower of M. flaviflorus. FFiigguurree 55. The butterfly Phoebisphilea on flowers of Micranthocereus flaviflorus. FFiigguurree 66. Males of Chlorostilbon aureoventris visiting flower ofM. streckeri. FFiigguurree 77. Males of Chlorostilbon aureoventris on flower of M. streckeri. Note the presence of pollengrains on the bill of the hummingbird. Photos by E.R. Pansarin.

4 5

6 7

Bradleya 24/2006 45

FFiigguurree 88. The hummingbird Phaethornis squalidus visiting flower of M. steckeri. FFiigguurree 99. The hesperid Vettius sp.(arrow) on flowers of M. streckeri. FFiigguurree 1100. The hawkmoth Agrius cingulatus visiting a flower of M. purpureus.Note the extend proboscis being introduced in the perianth. FFiigguurree 1111. The hawkmoth Erynnyis alope visiting aflower of M. purpureus. Note the extend proboscis being introduced in the perianth. Photos 8 & 9: E.R. Pansarin;10 & 11: L.Y.S. Aona.

8 9

10 11

Bradleya 24/200646

anthers and the stigma when collecting floral

nectar. The visitor prevented access by other

individuals of the same species to the population

of plants which it defended.

The butterfly Phoebis philea Johansson

(Figure 5) was occasionally observed visiting M.

flaviflorus flowers during the hottest hours of the

day (12 to 3 p.m.), when it collected nectar and

contacted the sexual parts of the flower. The bee

Trigona spinipes Fabricius was observed visiting

flowers of M. flaviflorus mainly from 10.30 to 11

a.m. and from 2 to 5 p.m., when it collected pollen

directly from the anthers, often damaging both

anthers, perianth-segments and floral tube, but

without contacting the stigma.

Flowers of M. streckeri were also pollinated by

Chlorostilbon aureoventris (Figures 6 & 7). In

this species the females were more frequent as

pollinators than males. The visits occurred

between 6 a.m. and 4 p.m., being more frequent

in the morning and occuring in intervals of

approximately 30 minutes, rarely up to 60 min-

utes. In the afternoon the visits were rare and

took place at intervals of 1hour 10 minutes,

approximately. Females of C. aureoventris pre-

sented the same territorialist behaviour observed

in males in M. flaviflorus, mostly during the

morning, when they defended the population

from males.

The hummingbird Phaethornis squalidus

Temminck was sporadically observed pollinating

M. streckeri flowers in late afternoon (Figure 8),

in a similar frequency to that of Chlorostilbon

aureoventris (t=0.896, P=0.394, Figure 12); birds

of this species were also chased away by females

of C. aureoventris. All hummingbird species had

the pollen grains deposited on the bill. In M. flav-

iflorus and M. streckeri, the visits by both species

of hummingbird to each flower were brief (c. 2

seconds). In most visits both hummingbirds visit-

ed more than one flower of each plant.

Some insects, like the skipper Vettius sp.

(Lepidoptera: Hesperiidae: Hesperiinae) species

(Figure 5), occasionally visited M. streckeri flow-

ers along the day, collected nectar and sometimes

touched the sexual parts of the flower with their

proboscis, being considered occasional pollina-

tors. Honey bees, Apis melifera, were observed on

flowers of M. streckeri mainly in the morning,

when they visited more than one flower of each

individual, or even flowers of the same cephali-

um. They landed at the apex of the floral-tube

and collected large amounts of pollen directly

from the anthers, sometimes causing anther

damage, and rarely contacted the stigma, thus

acting mainly as pollen robbers. Trigona spinipes

was also observed visiting flowers of M. streckeri

at the same period of the day and presenting sim-

ilar behaviour to that observed with M. flavi-

florus. Other occasional visitors were some non-

identified ants, beetles and caterpillar species,

which were observed cutting (ants) and eating

(beetles and caterpillars) floral parts.

Flowers of M. purpureus were visited by

the bat Lonchophylla mordax Thomas

(Phyllostomidae, Glossophaginae), which was

observed after dusk until 5 a.m., in intervals of

30–60 minutes, often approaching the plant from

the same direction of the cephalium, hovering in

front of the flowers and visiting different individ-

uals at each bout. During its visits, this bat intro-

duced its head inside the floral-tube, touching

the stigma and receiving the pollen grains on the

head, neck and shoulders. Lonchophylla mordax

also visited flowers of Encholirium brachypodum

L. B. Sm. & Read (Bromeliaceae) in a higher fre-

quency (intervals of 5–30 minutes) than that

observed for M. purpureus, but displaying a sim-

ilar behaviour.

The sphingids Agrius cingulata Fabricius

Corolla NectarSpecies

Length (mm) Diameter (mm) Vol (µl) Conc (%)

M. flaviflorus 12.35 ± 0.99b 1.76 ± 0.25b 5.17 ± 2.25b 23.33 ± 1.28b

M. streckeri 13.09 ± 1.23c 1.85 ± 0.18b 7.3 ± 3.8b 19.3 ± 1.83c

M. purpureus 31.88 ± 1.87a 16.35 ± 1.49a 143.81 ± 49.32a 21.18 ± 1.54a

TTaabbllee 11. Floral morphometrics and nectar features (mean ± sd for both) of three species ofMicranthocereus in northeast Brazil. Different letters in the same column indicate statistically different data.Vol.: volume, Conc.: concentration.

Bradleya 24/2006 47

(Figure10), Erynnyis alope Drury (Figure11),

Erynnyis ello L. (Sphingidae) were observed vis-

iting the flowers of M. purpureus, between 9 p.m.

and 4.30 a.m., with a peak between 9 p.m. and 12

a.m. (Figure 13). The hawkmoths approached the

flower and introduced the proboscis into the nec-

tar chamber, hovering at variable distances in

front of the flower. Photographs of moths forag-

ing at flowers reveal thick deposits of pollen

along their proboscis. The hawkmoths sometimes

touched the flowers with their forelegs, mainly E.

ello, with visits lasting up to three seconds. All

hawkmoths displayed a similar visitation pat-

tern, visiting the flowers more or less in the same

sequence and at intervals varying from 5–30

minutes, rarely up to 60 minutes. Agrius cingu-

lata was the most commonly observed visitor,

with visits lasting up to 15–20 seconds while

making circular movements with the proboscis.

Frequency of visits of sphingids was greater than

that of the bats (t = -2.24, P=0.02, Figure 13).

During anthesis a large number of small bee-

tles were found inside the flowers of M. pur-

pureus, remaining there even after flower senes-

cence. They were never seen flying from flower to

flower or touching the stigma. It was not possible

to observe what kind of floral resource these

insects explored. The flowers of M. purpureus

were also visited by the hummingbirds

Chlorostilbon aureoventris in the late afternoon

of the first day and Augastes lumachellus Lesson

in the early morning of the following day.

However, the hummingbird visits were rare and

it was not possible to observe whether contact of

anthers or stigmas occurred. Apis melifera and

Trigona spinipes were observed between 5–8 a.m.

and 4 and 5 p.m. (Figure 13), respectively, dis-

playing the same behaviour as was observed with

M. flaviflorus and M. streckeri (Figure 12).

DDiissccuussssiioonn

Most floral features of M. streckeri and M. flavi-

florus are similar to those displayed by species

pollinated by hummingbirds in tropical commu-

nities, such as the easily accessible and unscent-

ed flowers, with tubular and conspicuously

coloured perianth, clear separation between flo-

ral resource (nectar) and sexual parts and nectar

with a relatively low concentration of sugars

(Faegri & van der Pijl, 1980; Arzimendi &

Ornelas, 1990; Araujo, 1996, Sazima et al., 1996;

Locatelli & Machado, 1999b; Buzatto et al., 2000;

Castro & Oliveira, 2001, 2002; Castro & Araujo,

2004), including Cactaceae species (Scogin, 1985).

The short-tubed flowers of M. flaviflorus and

M. streckeri allow the visits of both short- and

long-billed visitors, like Chlorostilbon aureoven-

tris and Phaethornis squalidus, respectively

(Grantsau, 1989) however only M. streckeri was

visited by both species. The absence of P.

squalidus on M. flaviflorus flowers may be relat-

ed to the lack of forest habitats near the studied

population, since this species is a typical pollina-

tor in Atlantic forests in Brazil (Buzato et al.,

2000). This hummingbird seemed to prefer indi-

viduals of M. streckeri located in areas at lower

elevations, which are close to a wooded area. The

period in which P. squalidus and Trigona spinipes

visited M. streckeri flowers (after 2 p.m.), and

that in which T. spinipes visited M. flaviflorus

flowers coincided with the decrease in the num-

ber of C. aureoventris visits, a strategy that prob-

ably minimizes the chances of being attacked by

this hummingbird.

It was observed in the populations of

Micranthocereus streckeri that Phaethornis

squalidus invades the territory of Chlorostilbon

aureoventris after 11 a.m. (Figure 12). According

to Buzato et al. (2000), hermit hummingbirds

such as P. squalidus are the major pollinators of

hummingbird-pollinated of floras in Brazilian

forests. Phaethornis squalidus visited the plants

that occur near to the valley, nearby the forested

area. This behaviour might be related with the

visits decrease of C. aureoventris after 3 p.m. and

the visits increase of P. squalidus.

The decrease in the frequency of visits of

Chlorostilbon aureoventris to the flowers of M.

flaviflorus after 2 p.m. could be explained by the

presence of a sympatric Cactaceae species,

Melocactus paucispinus Heimen. & R. J. Paul,

whose flowers opened approximately at 2 p.m.

and were also visited by C. aureoventris.

However, it is necessary to test if this humming-

bird really prefers M. paucispinus flowers in com-

parison to those of M. flaviflorus.

The visiting behaviour of Chlorostilbon aure-

oventris to the flowers of M. flaviflorus and M.

streckeri revealed two types of feeding strategies:

territoriality (sensu Feinsinger, 1978; Stiles,

1981) and traplining. The traplining strategy

favours cross-pollination because it maximizes

pollen dispersion among different individuals

(Janzen, 1971), whereas the territorialist behav-

iour may reduce pollen flow in a population

(Linhart, 1973). The occurrence of these two

types of foraging behaviour (territorialist and

traplining) was also recorded for C. aureoventris

Bradleya 24/200648

in the flowers of Melocactus zehntneri (Britton &

Rose) Luetzelb. and Opuntia palmadora Britton

& Rose by Locatelli & Machado (1999b).

The protandry observed in M. flaviflorus and

M. streckeri is considered a reproductive strategy

that minimizes the interference between male

and female functions as well as the chances of

self-pollination (Webb & Lloyd, 1986). Protandry

was not found in M. purpureus, where the posi-

tion of the stigma (adaxial or lateral) in relation

to the stamens changed from adaxial or lateral to

central in the flower’s lifespan.

Flowers of M. purpureus present some typical

chiropterophilous features such as pale colour, a

short floral tube with wide aperture, nocturnal

anthesis and large amounts of nectar (Vogel,

1969; Faegri & van der Pijl, 1980). There is evi-

dence that the presence of a lateral sunken

cephalium, composed by congested, hairy flower-

bearing areoles, forming a cushion-like structure

is related with the protection of bat’s wings dur-

ing pollination (Zappi, 1994). The exerted posi-

tion of the stigma of M. purpureus seems to

favour cross-pollination because it is the first

reproductive part to be touched by the floral vis-

itors (Sazima & Sazima, 1975). However, a

6

3

0

8-9 9-10 10-11 11-12 12-13 13-14 14-15 15-16 16-17

Time Interval

Nu

mb

er

of

Vis

its

FFiigguurree 1122. Frequency of visiting bouts of M. flaviflorus and M. streckeri pollinators in NE Brazil. Males ofChlorostilbon aureoventris on flowers of M. flaviflorus (hatched bars); Phaethornis squalidus (grey bars) and maleof C. aureoventris (black bars) on M. streckeri flowers.

12

12

8

6

4

2

0

17-18 18-19 19-20 20-21 21-22 22-23 23-24 24-01 01-01 02-03 03-04 04-05 05-06

Time Interval

Nu

mb

er

of

Vis

its

FFiigguurree 1133. Frequency of visiting bouts of M. purpureus pollinators in NE Brazil. Sphingids (hatched bars),Loncophylla mordax (white bars), Chlorostilbon aureoventris (black bars) and Augastes lumachellus (grey bars).

Bradleya 24/2006 49

relatively low frequency of visits by bats was

recorded. The horizontally disposed position of

the flowers, as well as its presence at only on one

side of the plants of M. purpureus plants are fea-

tures expected in chiropterophilous species

(Vogel, 1969, Sazima et al., 1995; Machado et al.,

1998), because it seems that the one-side presen-

tation of the flowers facilitates their access by

bats, which are less able to maneuver in flight

than bees or hummingbirds. The low number of

flowers and sweet scent presented during the

anthesis by M. purpureus was found in bat-polli-

nated species in general (Sazima & Sazima,

1978; Machado et al., 1998; Sazima et al., 1999)

as well as in other bat-pollinated Cactaceae

species (Locatelli et al., 1997).

The regular paths coupled with the intervals

between visiting bouts observed for Lonchophylla

mordax visits to M. purpureus indicate a trapline

behaviour, as has been recorded for

Glossophagine species when feeding on flowers

(Baker, 1973; Fleming, 1982; Sazima et al., 1999).

This foraging pattern was already recorded in

several studies on bat-pollinated flowers in the

Brazilian Atlantic rainforest (Sazima et al., 1994,

Machado et al., 1998; Sazima et al., 1999),

“restinga” (Locatelli et al., 1997) and for L. boker-

manii in “campo rupestre” (Sazima et al., 1989).

The flowers of bromeliad Encholirium brachypo-

dum are in the great number (c.30 flowers/inflo-

rescence daily) than M. purpureus and have dis-

agreeable odour, more typical of bat-pollinated

species. These characters observed in E. brachy-

podium at the study site may partially explain

the preference of the L. mordax for the bromeliad

and the irregular intervals in feeding bouts on M.

purpureus.

Despite the hawkmoths being generally con-

sidered less efficient and less important pollina-

tors than bats in chiropterophilous species (sensu

Baker et al., 1971; Sazima & Sazima, 1978;

Sazima et al., 1994), these insects were more fre-

quently observed visiting M. purpureus flowers

than bats. These results indicate that M. pur-

pureus may have, at the sudy site, a mixed bat-

hawkmoth pollination system, similarly to the

one described for Lafoensia densiflora Pohl

(Silberbauer-Gottsberger & Gottsberger, 1975)

and for Cereus peruvianus auctt. [=C. hildmanni-

anus K. Schum.] (Silva & Sazima, 1995). In fact,

M. purpureus seems to present floral features

such as the flower odour, which is weak and

sweet, rather than strong and disagreeable that

are somewhat ambiguous between bat and hawk-

moth syndromes, suggesting an adaptation to

attract both pollinator types. Moreover, the

traplining strategy presented by many hawk-

moth species (Janzen, 1971), that was also

observed in this study, coupled with their quick

movements and long flight distances (Linhart &

Mendenhall, 1977), favour cross-pollination.

Despite the frequent presence of beetles with-

in the flowers of Micranthocereus purpureus,

similarly observed in other species of Cactaceae

(Silva & Sazima, 1995; Locatelli et al., 1997),

some studies suggested that these insects are not

important pollen vectors for most cacti species

(Grant & Hurt, 1979), but seem to act only as

robbers (Locatelli et al., 1997). The humming-

birds and bees that were observed contacting

anthers and stigma during their visits to M. pur-

pureus flowers should not be considered pollina-

tors because no stigma receptivity was observed

in these periods of anthesis (Figure 13).

Moreover, the flowers had nearly empty anthers

when visited by Augastes lumachellus Lesson,

which was observed only once; this Trochilidae

species was observed using M. purpureus hairs

for building its nest (Machado et al., 2003). The

potential for using both nocturnal and diurnal

pollinators is known in Cactaceae (McGregor et

al., 1962) and in other chiropterophilous

angiosperms (Buzato et al., 1994; Sazima et al.,

1994).

The range of nectar concentration of M. pur-

pureus was slightly higher than the values

recorded for some Neotropical bat-pollinated

species (5%–29%, often 15%–17%, von Helversen,

1993; Sazima et al., 1999). Scogin (1985) com-

pared nectar analyses in some Cactaceae species

as 22–30%, 15–34% and 17–26%, for those

respectively pollinated by hummingbirds, moths

and bats. The value found for M. purpureus was

similar to that found in other Brazilian bat-polli-

nated Cactaceae (Locatelli et al., 1997) and in

species of other families in Brazil (Sazima et al.,

2003). The present study found overlapping val-

ues of sugar concentration between

Micranthocereus, with the two hummingbird pol-

linated species (M. flaviflorus and M. streckeri) at

each range of the spectrum, while the bat polli-

nated M. purpureus had intermediate values

between the two (Table 1).

It was also found that the range of variation

in sugar concentrations in Micranthocereus may

favour relationships with less specific pollinators

than was initially expected. Tribe Cereeae

(Taylor & Zappi, 2004) comprises several closely

Bradleya 24/200650

related genera, each one with more than one pol-

linator and sometimes displaying gradients

between pollination syndromes. For example,

Stephanocereus and Coleocephalocereus are like-

ly to be pollinated by bats and hummingbirds,

and species of Pilosocereus are pollinated by bats

and hawkmoths was studied by Locatelli et al.

(1997), Locatelli & Machado (1999a) and E. A.

Rocha, pers. com.). Our results show a remark-

able variability in the flower biology within the

genus Micranthocereus.

AAcckknnoowwlleeddggeemmeennttss

We thank Dr. Nigel Taylor and Dr. Volker

Bittrich for kindly read the manuscript, Dr. Keith

J. Brown for identification of the species sphin-

gids, Dr. Ivan Sazima and Dr. Marlies Sazima for

identification of the bat species, Ludmila

Mickeliunas and Renato P. Oliveira for their

assistance in the field studies and Rogério Lupo

for the illustrations. This study is part of a

Master thesis by the first author for the post-

graduation course in Plant Biology at the

‘Universidade Estadual de Campinas’ (São Paulo,

Brazil). This work was supported by the

Research Support Foundation of São Paulo State

- FAPESP (process no. 00/00369-7).

RReeffeerreenncceess

AONA, L. Y. S. (2003). Caracterização e

delimitação do gênero Micranthocereus

Backeb. (Cactaceae) baseados em caracteres

morfológicos e moleculares. M. S. Thesis,

Universidade Estadual de Campinas, SP.

ARAÚJO, A. C. (1996). Beija-flores e seus recursos

florais numa área de planície costeira do

litoral norte de São Paulo. M. S. Thesis,

Universidade Estadual de Campinas, SP.

ARZIMEDI, M. C. & ORNELAS, J. F. (1990).

Hummingbirds and their flower resources in

a tropical dry forest in Mexico. Biotropica 2222:

172–180.

BAKER, H. G., CRUDEN, R. W. & BAKER, I. (1971).

Minor parasitism in pollination biology and

its community function: the case of Ceiba

acuminata. BioScience 2211: 1127–1129.

BAKER, H. G. (1973). Evolutionary relationships

between flowering plants and animals in

American and Africa tropical forests. In

Meggers, B. J., Ayensu, E. S., & Duckworth,

W. D. (Eds.), Tropical forest ecosystems in

Africa and South America: A comparative

review. Smithsonian Institute Press,

Washington, DC., pp. 145–159.

BARTHLOTT, W. & HUNT, D. (1993). Cactaceae. In

Kubitzki, K., Rohwer L. & Bittrich, V. (Eds.),

The families and genera of vascular plants,

Vol. II. Springer, Berlin, pp. 161–197.

BIANCHI, M. B., GIBBS, P. E., PRADO, D. E. &

VESPERINI, J. L. (2000). Studies on the breed-

ing systems of understorey species of a Chaco

woodland in NE Argentina. Flora 119955:

339–348.

BOYLE, T. H. (1996). Characteristics of self-incom-

patibility in Schlumbergera truncata and S.

buckleyi (Cactaceae). Sex. Pl. Repro. 99: 49––53.

BUZATO, S., SAZIMA, M. & SAZIMA, I. (1994).

Pollination of three species of Abutilon

(Malvaceae) intermediate between bat and

hummingbird flowers syndromes. Flora 118899:

227––334.

BUZATO, S., SAZIMA, M. & SAZIMA, I. (2000).

Hummingbird-pollinated floras at three

Atlantic forest sites. Biotropica 3322: 824–841.

CASTRO, C. C. & OLIVEIRA, P. E. (2001).

Reproductive biology of the protandrous

Fernandusa speciosa Pohl (Rubiaceae) in

southeastern Brazil. Rev. Bras. Bot. 2244:

167–172.

CASTRO, C. C. & OLIVEIRA, P. E. (2002).

Pollination biology of distylous Rubiaceae in

the Atlantic rain forest, SE Brazil. Plant Biol.

55: 640–646.

CASTRO, C. C. & ARAUJO, A.C. (2004). Distyly and

sequential pollinators of Psychotria nuda

(Rubiaceae) in the Atlantic rain forest, Brazil.

Plant Syst. Evol. 224444: 131–139.

FEINSINGER, P. (1978). Community organization

among neotropical nectar-feeding birds. Amer.

Zool. 1188: 779–795.

FAEGRI, K. & VAN DER PIJL, L. (1980). The princi-

ples of pollination ecology. 3rd ed. (Reprint

with revisions), Pergamon Press, New York.

FLEMING, T. H. (1982). Foraging strategies in

plant-visiting bats. In: Kunz, T. H. (Ed.),

Ecology of bats. Plenum Press, New York., pp.

287–325.

FLEMING, T. H., TUTLE, M. D. & HORNER, M. A.

(1996). Pollination biology and the relative

importance of nocturnal and diurnal pollina-

tors in three species of Sonoran Desert colum-

nar cacti. Southwest. Nat. 4411: 257–269.

GRANT, K. A. & HURT, P. D. (1979). Pollination of

the southwestern American opuntias. Pl.

Syst. Evol. 113333: 15–28.

GRANTSAU, R. (1989). Os beija-flores do Brasil.

Expressão e Cultura, Rio de Janeiro.

Bradleya 24/2006 51

HARBER, W. A. & FRANKIE, G. W. (1989). A tropical

community: Costa Rican community dry

forest Sphingidae. Biotropica 2211: 155–172.

HOLLAND, J. N.& FLEMING, T. H. (1999).

Mutualistic interactions between Upiga

virescens (Pyralidae), a pollinating seed-con-

sumer, and Lophocereus schottii (Cactaceae).

Ecology 8800: 2074–2084.

HUNT, D. R. & TAYLOR, N. P. (1990). The genera of

Cactaceae: progress towards consensus.

Bradleya 88: 85–107.

JANZEN, D. H. (1971). Euglossine bees as long-dis-

tance pollinators of tropical plants. Science

117711: 203–205.

LINHART, Y. S. (1973). Ecological and behavioral

determinants of pollen dispersal in hummin-

bird-pollinated Heliconia. Am. Nat. 110077:

511–525.

LINHART, Y. S. & MENDENHALL, J. A. (1977). Pollen

dispersal by hawkmoth in Lindenia rivalis

Benth. population in Beliza. Biotropica 99:

143.

LOCATELLI, E., MACHADO, I. C. S. & MEDEIROS, P.

(1997). Floral biology and pollination in

Pilosocereus catingicola (Cactaceae) in

Northeastern Brazil. Bradleya 1155: 28–34.

LOCATELLI, E. & MACHADO, I. C. S. (1999a). Floral

biology of Cereus fernambucensis: a sphin-

gophilous cactus of restinga. Bradleya 1177:

86–94.

LOCATELLI, E. & MACHADO, I. C. S. (1999b).

Camparative study of the floral biology in two

ornithophilous species of Cactaceae:

Melocactus zehntneri and Opuntia

palmadora. Bradleya 1177: 75–85.

MACHADO, C. G., MOREIRA, T. A., NUNES, C. E. C.

& ROMÃO, C. O. (2003). Use of

Micranthocereus purpureus (Guerke) F. Ritter

(Cactaceae) hairs in nests of Augastes

lumachellus Lesson (Trochilidae, Aves).

Sitientibus sér. Ciên. Biol. 33: 131–132.

MACHADO, I. C. S., SAZIMA, I. & SAZIMA, M. (1998).

Bat pollination of the terrestrial herb

Irlbachia alata (Gentianaceae) in northeast-

ern Brazil. Pl. Syst. Evol. 220099: 231–237.

MACHADO, M. C. (1999). The cacti of Morro do

Chapéu, Bahia, Brazil. Brit. Cact. Succ. J. 1177:

203–213.

MCFARLAND, J. D., KEVAN, P. G. & LANE, M. A.

(1989). Pollination biology of Opuntia imbri-

cata (Cactaceae) in southern Colorado (USA).

Can. J. Bot. 6677: 24–28.

MANDUJANO, M. D. C, MONTANA, C., MENDEZ, I. &

GOLUBOV, J. (1998). The relative contributions

of sexual reproduction and clonal propagation

in Opuntia rastrera from two habitats in the

Chihuahuan Desert. J. Ecol. 8866: 911–921.

MCGREGOR, S. E., ALCORN, S. M. & OLIN, G.

(1962). Pollination and pollinating agents of

the saguaro. Ecology 4433: 259–267.

METZ, C., NERD, A. & MIZRAHI, Y. (2000). Viability

of pollen of two fruit crop cacti of the genus

Hylocereus is affected by temperature and

duration of storage. Hortscience 3355: 199–201.

NEGRON-ORTIZ,, V. (1998). Reproductive biology of

a rare cactus, Opuntia spinosissima

(Cactaceae), in the Florida Keys: Why is seed

set very low? Sex. Pl. Repro. 1111: 208–212.

NEWSTRON, L. E., FRANKIE, G. W. & BAKER, H. G.

(1994). A new classification for plant phenolo-

gy based on flowering patterns in lowland

tropical rain forest trees at La Selva, Costa

Rica. Biotropica 2266: 141–159.

PORSCH, O. (1939). Cactaceae. In: Druck, J. (Ed.),

Das Bestäubungsleben der Kakteen-blüte, II.

Cactaceae (DKG) 11993399: 81–142.

RADFORD, A. E., DICKINSON, W. C., MASSEY, J. R. &

BELL, C. R. (1974). Vascular plant systematics.

Harper & Tow Publishing, New York.

RAW, A. (1996). Territories of the ruby-topaz hum-

mingbird Chrysolampis mosquitus at flowers

of the “turk’s-cap” cactus, Melocactus sal-

vadorensis in the dry caatinga of the north-

eastern Brazil. Rev. Bras. Biol. 5566: 581–584.

RUIZ, A., SANTOS, M., SORIANO, P. J., CAVELIER, J.

& CADENA, A. (1997). Mutualistic relations

between the bat Glossophaga longirostris and

the columnar cacti in the arid region of La

Tatacoa, Colombia. Biotropica 2299: 469–479.

RUSCHI, A. (1986). Aves do Brasil, Beija-flores.

Expressão e Cultura, Rio de Janeiro.

SAHLEY, C. T. (2001). Vertebrate pollination, fruit

production, and pollen dispersal of

Stenocereus thurberi (Cactaceae). Southwest.

Nat. 4466: 261–271.

SAZIMA, I., VOGEL, S. & SAZIMA, M. (1989). Bat

pollination of Encholirium glaziovii, a terres-

trial bromeliad. Pl. Syst. Evol. 115588: 167–179.

SAZIMA, I., BUZATO, S. & SAZIMA, M. (1996). An

assemblage of hummingbird-pollinated

flowers in a montane forest in southeastern

Brazil. Bot. Acta 110099: 149–160.

SAZIMA, M. & SAZIMA I. (1975). Quiropterofilia em

Lafoensia pacari St. Hil. (Lythraceae), na

Serra do Cipó, Minas Gerais. Ciên. Cult. 2277:

404–416.

SAZIMA, M. & SAZIMA, I. (1978). Bat pollination of

the Passion flower, Passiflora mucronata, in

Bradleya 24/200652

Southeastern Brazil. Biotropica 1100: 100–109.

SAZIMA, M., SAZIMA, I. & BUZATO, S. (1994).

Nectar by day and night: Siphocampylus sul-

fureus (Lobeliaceae) pollinated by humming-

birds and bats. Pl. Syst. Evol. 119911: 237–146.

SAZIMA, M., BUZATO, S. & SAZIMA, I. (1995). Bat

pollination of Vrisea in southeastern Brazil.

Bromélia 22: 29–37.

SAZIMA, M., BUZATO, S. & SAZIMA, I. (1999). Bat-

pollinated flower assemblages and bat visi-

tors at two Atlantic forest sites in Brazil. Ann.

Bot. 8833: 705–712.

SAZIMA, M., BUZATO, S. & SAZIMA, I. (2003).

Dyssochroma viridiflorum (Solanaceae): a

reproductively bat-dependent epiphyte from

the Atlantic Rainforest in Brazil. Ann. Bot.

9922: 725–730.

SCHLINDWEIN, C. & WITTMANN, D. (1995).

Specialized solitary bees as effective pollina-

tors of south Brazilian species of Notocactus

and Gymnocalycium (Cactaceae). Bradleya

1133: 25–34.

SCHLINDWEIN, C. & WITTMANN, D. (1997). Stamen

movements in flowers of Opuntia (Cactaceae)

favour oligolectic pollinators. Pl. Syst. Evol.

220044: 179–193.

SCOBELL, S. A. & SCOTT, P. E. (2002). Visitors and

floral traits of a hummingbird-adapted cactus

(Echinocereus coccineus) show only minor

variation along an elevational gradient. Am.

Mid. Nat. 114477: 1–15.

SCOGIN, R. (1985). Nectar constituents of the

Cactaceae. Southwest. Nat. 3300: 77–82.

SILVA, W. R. & SAZIMA, M. (1995). Hawkmoth pol-

lination in Cereus peruvianus, a columnar

cactus from southeastern Brazil. Flora

119900:339–343.

SILBERBAUER-GOTTSBERGER, I. & GOTTSBERGER, G.

(1975). Über Shingophile Angiospermen

Brasiliens. Plant Syst. Evol. 112233: 157–184.

SOKAL, R. R., ROHLF, J. R. F. (1969). Biometry: the

principles and practice of statistics in biologi-

cal research. W. H. Freeman, San Francisco.

STILES, F. G. (1981). Geographical aspects of bird-

flower coevolution, with particular reference

to Central America. Ann. Miss. Bot. Gard. 6688:

323–351.

SUZAN, H., NABHAN, G. P & PATTEN, D. T. (1994).

Nurse plant and floral biology of a rare night-

blooming cereus Peniocereus striatus

(Brandegee) F. Buxbaum. Conserv. Biol. 88:

461–470.

TAYLOR, N. P. & ZAPPI, D. (2004). Cacti of Eastern

Brazil. Royal Botanic Gardens, Kew.

TSCHAPKA, M., VON HELVERSEN, O. & BARTHLOTT,

W. (1999). Bat pollination of Weberocereus

tunilla, an epiphytic rain forest cactus with

functional flagelliflory. Plant Biol. 11: 554––559.

VIANA, M. L., ORTEGA, B. P., SARAVIA, M., BAO, E.

I & SSCHLUMPBERGER, B. (2001). Biologia flo-

ral y polinizadores de Trichocereus pasacana

(Cactaceae) en el Parque Nacional Los

Cardones, Argentina. Revist. Biol. Trop. 4499:

279––285.

VOGEL, S. (1969). Chiropterophilie in der neotro-

pischen Flora. Neue Mitteilungen II. Flora

115588: 185––222.

VOGEL, S. (1990). Radiacion adaptativa del sin-

drome floral en las familias neotropicais. Bol.

Acad. Nac. Cien. Córdoba Argentina 5599: 4––30.

VON HELVERSEN, O. (1993). Adaptations of flowers

to pollinationd by Glossophagine bats. In

Barthlott, W. Naumann, C. M., Schimidt-

Loske, K. & Schumann, K. L. (Eds.), Animal-

Plant interactions in tropical environments.

Museum Alexandre König, Bonn, pp. 41–59.

WALLACE, R. S. & COTA, J. H. (1996). An intron

loss in the chloroplast gene rpoCi supports a

monophyletic origin for the subfamily

Cactoideae. Curr. Genet. 2299: 275–281.

WEBB, C. J., LLOYD, D. G. (1986). The avoidance

of interference between the presentation of

pollen and stigmas in Angiosperms. I.

Dichogamy. New Zeal. J. Bot. 2244: 135––162.

ZAPPI, D. C. (1994). Pilosocereus (Cactaceae): The

genus in Brazil. Succ. Pl. Res. 33: 1–160.